The Silver Lining of a Viral Agent: Increasing Seed Yield and Harvest Index in Arabidopsis by Ectopic Expression of the Potato Leaf Roll Virus Movement Protein

Abstract

Ectopic expression of viral movement proteins (MPs) has previously been shown to alter plasmodesmata (PD) function and carbon partitioning in transgenic plants, giving rise to the view of PD being dynamic and highly regulated structures that allow resource allocation to be adapted to environmental and developmental needs. However, most work has been restricted to solanaceous species and the potential use of MP expression to improve biomass and yield parameters has not been addressed in detail. Here we demonstrate that MP-mediated modification of PD function can substantially alter assimilate allocation, biomass production, and reproductive growth in Arabidopsis (Arabidopsis thaliana). These effects were achieved by constitutive expression of the potato leaf roll virus 17-kD MP (MP17) fused to green fluorescent protein (GFP) in different Arabidopsis ecotypes. The resulting transgenic plants were analyzed for PD localization of the MP17:GFP fusion protein and different lines with low to high expression levels were selected for further analysis. Low-level accumulation of MP17 resulted in enhanced sucrose efflux from source leaves and a considerably increased vegetative biomass production. In contrast, high MP17 levels impaired sucrose export, resulting in source leaf-specific carbohydrate accumulation and a strongly reduced vegetative growth. Surprisingly, later during development the MP17-mediated inhibition of resource allocation was reversed, and final seed yield increased in average up to 30% in different transgenic lines as compared to wild-type plants. This resulted in a strongly improved harvest index. The release of the assimilate export block was paralleled by a reduced PD binding of MP17 in senescing leaves, indicating major structural changes of PD during leaf senescence.

Increased Expression of a Phloem Membrane Protein Encoded by NHL26 Alters Phloem Export and Sugar Partitioning in Arabidopsis

“…The localization of NHL26 in the PD and the blocking of sugar export by its overaccumulation suggest a role for NHL26 in the opening of PD. This would be consistent with the phenotypic changes in overexpressing plants, resembling those observed in transgenic plants constitutively producing movement proteins, also leading to a disruption of sugar allocation (Balachandran et al, 1995;Olesinski et al, 1996;Almon et al, 1997;Herbers et al, 1997;Hofius et al, 2001;Shalitin et al, 2002;Rinne et al, 2005;Kronberg et al, 2007). The simplest explanation is that the overaccumulation of NHL26 modifies PD permeability.…”

Callose deposition in the phloem plasmodesmata and inhibition of phloem transport in citrus leaves infected with “Candidatus Liberibacter asiaticus”

“…b Autoradiograph of grapefruit leaves 0, 24, and 48 h after 14 CO 2 labeling. Levels of radioactivity are stronger in Las + leaves than in Las − leaves at each time point aberrant seed/fruit development (Russin et al 1996;Rinne et al 2005;Kronberg et al 2007;Ma et al 2008;Zavaliev et al 2010). These phenotypes are analogous to the symptoms of HLB infection (Brlansky et al 2010).…”

Choline transporter‐like1 (CHER1) is crucial for plasmodesmata maturation in Arabidopsis thaliana

“…It fulfills the three key qualifications for viral MP, namely RNA binding capability, localisation to PD and the ability to increase the PD size exclusion limit (SEL) (Tacke et al, 1991;Schmitz et al, 1997;Hofius et al, 2001). High levels of constitutive MP17 expression with a C-terminal GFP fusion (p35S: MP17-GFP) in Arabidopsis lead to growth retardation, development of chlorosis and an export block of carbohydrates in source leaves (Kronberg et al, 2007). MP17 localises to complex PD in source tissues but not to structurally dissimilar simple PD of developing tissues, where it is degraded by the 26S proteasome.…”